In 1965 Faulkner was appointed Parliamentary Secretary to the Minister for the Gaeltacht by the Taoiseach, Seán Lemass. He was appointed to the Cabinet by the new Taoiseach Jack Lynch in 1968, and served in every Fianna Fáil-led government until 1980. During the Arms Crisis he was a Lynch loyalist. He was one of a number of senior TDs who organised the assembly of TDs and Senators in Dublin Airport to welcome Lynch home from the United States after the defendants had been found not guilty at the Arms Trial. Nine years later in 1979 one of those defendants, Charles Haughey, was elected Taoiseach. Faulkner was retained in the Cabinet until 1980 when he was elected Ceann Comhairle of Dáil Éireann.

Following the election of a new Ceann Comhairle immediately after the 1981 general election, he retired to the backbenches before retiring completely from politics at the 1987 general election. In a Dáil career that spanned thirty years, his most notable achievements include the introduction of the legislation to establish two commercial semi-State companies, An Post and Telecom Éireann. Faulkner was subsequently appointed to the Council of State by President Patrick Hillery in 1990.